Journal of Bioresource Management

Volume 8 Issue 1 Article 2

Spatio-Temporal Variation Patterns of Community in the Oasis Ecosystem of the North of Algerian Sahara

Lasad Chiheb Department of Natural and Life Sciences, Faculty of Sciences, M’Sila University, M’Sila, Algeria., [email protected]

Bensaci Ettayib Biology, Water and Environment Laboratory (LBEE), University Mai Guelma, Guelma, Algeria, [email protected]

Nouidjem Yassine Department of Natural and Life Sciences, Faculty of Sciences, M’Sila University, M’Sila, Algeria, [email protected]

Hadjab Ramzi Life and Nature Sciences Department, University of “Larbi Ben M'hidi”, OumEl Bouaghi, [email protected]

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Recommended Citation Chiheb, L., Ettayib, B., Yassine, N., & Ramzi, H. (2021). Spatio-Temporal Variation Patterns of Bird Community in the Oasis Ecosystem of the North of Algerian Sahara, Journal of Bioresource Management, 8 (1). DOI: https://doi.org/10.35691/JBM.1202.0161 ISSN: 2309-3854 online (Received: Nov 4, 2020; Accepted: Dec 16, 2020; Published: Jan 27, 2021)

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This article is available in Journal of Bioresource Management: https://corescholar.libraries.wright.edu/jbm/vol8/ iss1/2 Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

SPATIO-TEMPORAL VARIATION PATTERNS OF BIRD COMMUNITY IN THE OASIS ECOSYSTEM OF THE NORTH OF ALGERIAN SAHARA

LASAD CHIHEB 1,2, BENSACI ETTAYIB 1,2 , NOUIDJEM YASSINE 1 AND HADJAB RAMZI 3

1Department of Natural and Life Sciences, Faculty of Sciences, M’Sila University, M’Sila, Algeria 2 Biology, Water and Environment Laboratory (LBEE), University Mai Guelma, Guelma, Algeria 3Life and Nature Sciences Department, University of “Larbi Ben M'hidi”, OumEl Bouaghi

Corresponding author’s email: [email protected]

ABSTRACT

The spatial and temporal variation patterns of were investigated in the Oasis ecosystem of the North of Algeria Sahara. This contribution aimed to investigate the poorly studied bird fauna of Bousaâda oasis. The direct observation method was used for bird counts, adopted only during the breeding period. A total of 53 species of birds from 29 families and 16 orders were assessed in the different habitats of the Oasis (palm, fruit trees and, cultivated crops). The Passeriformes order was the most abundant represented by 35 species and 16 families. The relative abundance and species richness were recorded during our study period over different seasons and thought that whole surveyed stations represent all the oasis habitats. The Boussaâda oasis holds 18 resident-breeders which is a transit zone for a number of migratory birds i-e 14 and 10 species for summer and winter migrants respectively) and11 occasional visitor ones. These results confirmed the positive effects of stations and seasons on the richness and abundance of birds of Bousaâda oasis.

Keywords: Oasis, bird, spatio-temporal, Algeria. the Ramsar Convention, oases are INTRODUCTION considered a type of inland wetlands (Ramsar, 2007). However, the ecological Biodiversity studies attracted the characteristics of oases in Algeria varied world’s attention to find its impacts on between regions following their humans and provide parallel ecosystem geographic location. Although, the services (Harrington et al., 2010). During ecosystems of arid and desert regions has the last century, reduction in biological very peculiar biodiversity related to locale diversity has directly affected the human biotope and climate (McGinley, 2007) activities (Heywood and Watson, 1995). particularly birds (Roshier et al., 2001; The oasis is considered as a fragile Mwaura, 2010; Chenchouni, 2012). ecosystem of the arid climate. The The avifauna of Algerian oases landscape mainly relies on the components were reported by Heim de Balsac and of a desert-oasis-river (Yang et al., 2010). Mayaud (1962) and Dupuy (1966) Over the centuries, oases have played a followed by updated data (Ledant et al., key role in the local socio-economic 1981; Isenmann and Moali, 2000; development and in the ensuring of Samraoui, 2008). In southern Tunisia, ecological balance. Multiple factors both many surveys were undertaken on the natural and human have seriously affected diversity and distribution of this avifauna the oasis ecosystem during the last century (Selmi et al.,2002). Some studies were (Botes and Zaid, 2002). available on birds of oases in Algeria Oases help study survey (Boukhemza, 1990; Chenchouni, 2012; biodiversity and their ecological Bensaci et al., 2013) but these were limited characteristics because of their key to few regions and were occasionally habitats (Chenchouni, 2012). According to observed.

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

The present study was Bird Surveys undertaken with the two basic objectives: i) to assess the bird diversity of the oasis Bird surveys were conducted located in arid climate differently to from March 2019 to March 2020 which previous studies on Oases of Sahara covered all seasons of the year, with three Desert; and ii) to evaluate the spatio- passes are performed in each station during temporal variation patterns of birds within each season, which normally can detect all Bousâada oasis. wintering, visitor passage and breeding species (Blondel, 1975). The most accurate MATERIAL AND METHODS and appropriate method is the territory- mapping method which is used for Study Area estimating the species richness and the avian communities abundance in open Bousâada (35° 12' 36.97"oN, 4° 10' o habitats (Bibby et al., 1992). 46.08" E) is a marvelous oasis, located in This approach based on the the centre of the northwardly located state assessment of all contacted birds and their of Algeria at an altitude of 602m above the abundances during a period of 15 minutes. sea level (Figure1). The oasis is delimited A pair of binoculars (8×42) and a field by three structural groups: high plains of guide book were also used to identify the the Algiers-Oran steppes to the north and species of birds observed. Counts were east, Saharan desert to the south, and performed in calm weather, avoiding harsh Saharan Atlas to the west (Kaabeche, weather, wind and bitter cold). For this 1990). The area has an arid climate (annual study total 19 census points (station) were mean temperature 25°C, average annual selected non-randomly on the basis of precipitation <185.8 mm) with dry season habitat type and their accessibility. extends all along the year. Overall, these stations located in four (4) studied regions: Zakat El-Kib (ZEK), Loulaj (LLJ), JnanLebtom 1 (JB1) and, JnanLebtom 2 (JB2) (Table 1). These regions have different habitat characteristics. Depending on their location, the surveyed stations are the subject of varied urban pressure and human disturbance. Phenological types used were (1) resident breeder (RB) species present all year with breeding proof; (2) winter visitor (WV) species observed exclusively during the rainy Figure 1: Study area location. season; (3) summer visitor (SV) migratory species in summer; (4) occasional visitor Bousâada oasis is the first one (OV) species that observed in the study encountered while heading from the region at least once (Isenmann and Moali, coastline to the Sahara Desert (Boutabba, 2000). 2013) Oasis is crossed by Oued Bousâada, During the study period the total flowing at the foot of a huge cliff used for numbers of species counted at each station irrigation. The landscape is dominated by were defined as species richness. palm trees (Phoenix dactylifera L.) mixed However, the species abundance with fruit trees and cultivated crops. Table 1: Characteristics of studied regions.

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

Region No. of stations Vegetation Species Richness (±SD) NDVI

ZEK1 4 47.00 ± 6.40 0.38 ± 0.03 JB 2-1 5 32.4 ± 7.68 0.23 ± 0.03 JB 1-1 5 37.00 ± 13.68 0.35 ± 0.04 LLJ-1 5 38.00 ± 6.80 0.29 ± 0.09

NDVI: The normalized difference vegetation index means the highest number of birds species RESULTS counted at different points during surveys. Specific Richness Data Analysis A total of 53 bird species, Statistical tests were performed representing 40 genera, 29 families and 16 using SPSS 17.0 with a significance level orders were recorded in the Oasis of of P ≤0.05. All means are shown ± Boussaâda from all surveyed stations standard error of mean unless stated (Table 1). Order Passeriformes has otherwise. represented the highest number of species We used parametric tests and (35; 16 families). Order Columbiformes ANOVA to test all variables,when the was represented by 4 species while orders normality (Kolmogorov–Smirnov test) and , and homoscedasticity (Levene test), the by two species each. variables were transformed by logarithm Other orders (11) were represented by only or a square-root transformation, the ones a single species, (Table 2). did not conform the requirements for parametric tests, before all analyses Spatial Richness and Abundance (Underwood, 1996). Variation of Birds A one-way multivariate analysis of variance (MANOVA) was performed to The species mean richness varied test the effect of stations and seasons on significantly between surveyed stations therichness and abundance of assessed (ANOVA: F1, 18= 7.76, P= 0.000). The birds. high mean richness value was recorded in The Shannon’s diversity index the JB1-2 (13.18±2.82) where the lower (퐻’=−∑푝푖 log 푝푖), where 푝푖: is the was marked in JB1-5 (5.18±3.06) (Table proportion of individuals belonging to the 3). The species mean abundance 푖: the species) was used to identify the훼- varied significantly between surveyed diversity of bird species in different stations (ANOVA: F1, 18= 6.79, P = stations (Magurran, 2004). High values of 0.000). The high abundance was recorded H' and low values of H' indicate high in the JB2-1 (80.18±41.91) where the species diversity (Krebs, 1999). lower was in JB1-5 (9.54±6.50) (Table 3) Equitability (Evenness), the one-way MANOVA confirmed the distribution of abundances among species statistically significant difference in was computed as J'= H'/lnS, whereas S is richness and abundance between stations, the number of species in each station (Magurran, 2004). Evenness was rangeing from 0 to 1 and all individuals were partitioned equally among species, as it approached 1 (Krebs, 1999).

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

Table 2: Taxonomic list of the bird species recorded at all the different surveyed stations in the Bousaâda oasis during 2019 to 2020.

Order Family Species Common Name Phenoloical Category Phoenicurus moussieri Moussier’s Redstart OV Phoenicurus ochruros WV Phoenicurus phoenicurus Redstart OV Oenanthe deserti Desert OV Muscicapidae Oenanthe leucura Black Wheatear RB Lusciniame garhynchos Nightingale SV Erithacus rubecula Robin WV Ficedula hypoleuca Pied Flycatcher SV Muscicapas triata SV Sylvia atricapilla Black cap WV Sylvia hortensis Western Orphean Warbler SV Sylvia melanocephala SardinianWarbler RB Phylloscopus collybita Chiff chaff WV Passeriformes Phylloscopidae Phylloscopus sibilatrix Wood Warbler SV Phylloscopus trochilus SV Chloris chloris Green RB Fringillidae Serinus serinus Serin RB Bucanetes githagineus OV Motacilla alba Pied WV Motacilla cinerea WV Anthustrivialis Tree Pipit OV Lanius elegans Great Grey WV Laniidae Lanius senator Woodchat Shrike SV Passer domesticus House Sparrow RB Passeridae Passer montanus Tree Sparrow RB Turdus merula Black bird RB Turdidae Turdus philomelos Song WV

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

Acrocephalidae Iduna opaca Western Olivaceous Warbler SV Paridae teneriffae African Blue RB Alaudidae Galerida cristata Crested RB Emberizidae Emberiza striolata Striolated RB Corvus corax Raven RB Hirundinidae Hirundo rustica SV Sturnidae Sturnus vulgaris WV Cisticolidae Cisticola juncidis Zitting Cisticola RB Streptopeliade caocto Collared Dove RB Streptopelia senegalensis Laughing Dove RB Columbiformes Streptopelia turtur Turtle Dove SV Columba livia RB Neophronpercnopterus EgyptianVulture SV Accipitriformes Circus aeruginosus Western Marsh OV Bubulcus Cattle RB Pelecaniformes Ardeidae Nycticorax nycticorax Black-crowned Night- OV Charadrius dubius Little Ringed SV Charadriiformes Scolopacidae ochropus Green Sand piper WV Ciconiiformes Ciconiidae Ciconia ciconia White SV Gruidae Grus grus OV Falco tinnunculus RB Strigiformes Strigidae Athenenoctua Little OV Bucérotiformes Upupidae Upupaepops RB Meropidae Merops apiaster Bee-eater SV Picidae Jynxtor quilla Wryneck OV Alectoris barbara Barbary OV

(RB=resident breeder, SV =summer visitor, OV: = occasional visitor, WV =winter visitor)

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

F (36, 378) = 6.37, p <.0005; Wilk's Λ = Similarly one-way MANOVA 0.378. suggest a statistically significant differences in richness and abundance Table 3: Spatial mean richness and abundance difference between seasons (F 36, 378 = variations of assessed birds. 6.37, p <.0005; Wilk's Λ = 0.378). Station Richness Abundance (Mean ± SD) (Mean ± SD) Table 4: Seasonal mean richness and abundance variations of assessed birds. JB1-1 5.82 ± 4.75 18.09 ±11.84 JB1-2 13.18 ±2.82 44.27 ±40.90 Season Richness Abundance JB1-3 8.45 ±4.03 28.64 ±18.40 (Mean ± SD) (Mean ± SD) JB1-4 6.45 ±2.84 12.91 ±5.28 Autumn 7.95 ± 2.87 27.92 ±25.76 JB1-5 5.18 ±3.06 9.55 ±6.50 Spring 9.82 ± 3.95 31.72 ± 23.82 JB2-1 12.82 ±2.68 80.18 ±41.91 Summer 8.75 ± 3.38 34.70 ±25.57 JB2-2 8.00 ±1.84 39.82 ±18.62 Winter 7.92 ± 3.30 53.50 ±53.57 JB2-3 6.73 ±2.24 39.82 ±23.37 JB2-4 7.18 ±1.83 50.64 ±30.02 Shannon-Weaver Diversity and Evenness JB2-5 7.09 ±1.22 52.91 ±30.33 (Equitability) Indexes LLJ1 11.00 ±4.05 33.18 ±44.27 LLJ2 7.45 ±3.08 10.09 ±8.29 The highest value of the Shannon diversity index was observed in the JB1-3 LLJ3 8.36 ±1.63 20.09 ±32.33 (3.64) and the lower of 2.34 was recorded 9.36 ±2.46 10.82 ±5.56 LLJ4 in the JB1-4 station (Fig 2). The maximum LLJ5 7.18 ±2.44 11.00 ±5.80 value of the equitability index was ZEK1 11.91 ±2.07 68.82 ±32.53 recorded in the LLJ5 station (0.77), where ZEK2 10.55 ±4.01 52.18 ±40.37 the minimum value was noted in the JB1-4 ZEK3 10.55 ±2.25 52.09 ±24.62 (0.53) (Figure 3). ZEK4 10.73 ±1.68 45.18 ±24.41 Phenological Status of Birds

Seasonal Richness and Abundance The avifauna of Bousâada Oasis is Variation of Birds dominated by resident breeder species (18 species), followed by summer visitor The species richness varied species (14 species), occasional visitor (11 significantly between seasons (ANOVA: species), and winter migrant (10 species) F = 3.65, P = 0. 013). The high mean 1,3 (Figure 4). richness value was recorded during spring (9.82±3.95) whereas the winter had the minimum richness (7.92±3.30) (Table 4). However, no significant difference in abundance was found between seasons (ANOVA: F1,3= 5.07, P = 0. 069).

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

4 3.5 3 2.5 2 1.5 1 0.5

0 Shannon Weaver & index

Station

Figure 2: Shannon-Weaver diversity index variation of birds of Bousaâda Oasis.

0.9

0.8 0.7 0.6 0.5 0.4 0.3 0.2 Equitability index 0.1 0

Station

Figure 3: Evenness (Equitability) index variation of birds of Bousaâda Oasis.

10 18

RB SV OV 11 WV

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Figure 4: Phenological status of birds of Bousaâda Oasis.

RB: Resident breeder, SV: Summer visitor, OV: Occasional visitor, WV: Winter visitor

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21

2013) and worldwide (Bonter et al., 2010). DISCUSSION These species are considered as the most abundant and the common birds in all The inventory of birds in Bousaâda oases of the Tunisian Sahara (Selmi., oasis suggests that 53 bird species, 2002). representing 7.66% of the Algerian birds Bousaâda oasis is known to have a (Isenman and Moali, 2000). However, in high anthropogenic pressure (urbanization, the Ziban region (Biskra, Algeria) Farhi high rate of ground water extraction, land and Belhamra (2012) identified 136 encroachment) which led to the loss of species representing 18 orders and 42 many habitats, affecting bird's richness and families (including waterbirds), of which abundance. Donnelly and Marzluff (2006) Passeriformes were represented by 58 confirmed that the increase in urban land species (12 families). Guezoul et al., cover badly effect the bird species richness (2013) reported 59 species present over a and result in its decrease. larger area, covering three different oases Assessed species represent of the Northern Algerian Sahara. different phenological status: 18 resident The assessed richness in the study breeder species (34%), followed by 14 area is lower than that reported in south summer visitor species (26%), 11 Tunisian oases,(Selmi,2002: 86 species, 13 occasional visitors (21%), and 10 winter families, 4 orders).Species richness at migrant species (19%). The dominance of Bousaâda oasis, was higher than that resident breeder species could be justified recorded by Guezoul et al. (2013) for by the heterogeneity of the micro-habitats different oasis (Biskra: 47, Oued Souf: 33 of oasis that contains palm and fruit trees and Ouargla: 44). and cultivated crops. Isenmann and Moali The highest richness of oases birds (2000) and Ledant et al., (1981), recorded in Algeria was recorded in Timimoun that the species, like, Phoenicurus region (SWAlgeria), where 100 species ochruros, Erithacus rubecula, Sylvia (12 orders, 28 families and 59 genera) atricapilla, Phylloscopus collybita, were described. Most of the species can be Motacilla alba, Motacilla cinerea, Lanius attributed to varied habitat sampled, such elegans Turdus philomelos, Sturnus as oases, salt lake, reeds, and suburban vulgaris, and Tringaochropus, as winter area (Boukhemza, 1990). visitor to Algerao oasis. Other species, Order Passeriformes is prominently like, Phoenicurus moussieri, Phoenicurus represented in all avian populations that phoenicurus, and Bucanetes githagineus are present in the oasis (66% of assessed are occasional visitors that use oasis as a species). This is in line with previous stopover point during their trans-Saharan studies on oases birds of Algeria (Farhi journey. These species stop on oases to and Belhamra, 2012; Guezoul et al., 2013). supply energy to be able to reach their The most of bird species in the surveyed wintering or breeding site (Lavee et al., oases were closely related to their 1991, Bairlein, 1992; and Biebach et al., phenology. 2000). During the monitoring many Abundance of some species, such species were presented in the most as feral pigeons, , swifts, and a surveyed stations such as :Hybrid sparrow, few other species that breed in walls Collared Dove, Laughing Dove, Turtle indicated increased urbanization. Thus, Dove, Rock Dove, Greenfinch and landscape transformation of the oasis Blackbird), some of these are known to during last decade has been indicated have an expansion of their distribution previously (Botes and Zaid, 2002; range over the Mediterranean basin Meddich et al., 2018).Significant special (Bergier et al., 1999; Bendjoudi et al., variation reveals the high quality of

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Chiheb et al. (2021). Spatio-Temporal Variation of Bird Community in Sahara. J Biores Manag., 8(1) : 11-21 habitats with high supply of seeds and Bendjoudi D, Chenchouni H, Doumandji productivity (Emlen, 1974). S, Voisin JF (2013). Bird The stations presented a high urban diversity in Plain Mitidja (N. pressure and human disturbance were Algeria) with emphasis on recorded a low species richness, which is dynamics of invasive and in confirmation of Chace and Walsh expanding species. Acrocephalus (2006) and Sandström et al., (2006). 33. Furthermore, The composition of Bensaci E, Saheb M, Nouidjem Y, vegetation in an area is closely associated Bouzegag A, Houhamdi M with the composition and variations of bird (2013). Biodiversité de communities and their abundance. l’Avifaune aquatique des Zones (Sewell and Catterall, 1998; White et al., Humides Sahariennes : Cas de la 2005 and Daniels and Kirkpatrick, 2006). Dépression d’Oued Righ Shannon and Weaver's index allow (ALGÉRIE). Physio-Géo – us to measure the complexity of a stand. A Géographie Physique et high value of this index indicates a Environnement VII 211-222. settlement in many species for a small Bergier P, Franchimont J, Thevenot M number of individuals. Conversely, a low (1999). Implantation et expansion value of the latter is either or a settlement géographique de deux espèces de characterized by a small number of species Columbidés au Maroc : La for many people, or to a settlement in Tourterelle turque which there is a dominant species. In other Streptopeliadecaocto et la words, he studied the equilibrium of Tourterelle mallee Streptopelia populations in an ecosystem. senegalensis. Alauda. 67: 23–36. Despite the rapid urbanization of Bibby CJ, Burgess ND and Hill DA Bousaâda region, this relevant diversity (1992). Bird census techniques. can help to support the conservation Academic Press, London. measures of native avian populations, Biebach H, Biebach I, Friedrich W, representing animportant biodiversity Heine G, Partecke J, Schmidl D hotspots which is located in the arid (2000). Strategies of region. migration across the Mediterranean Sea and the Sahara CONCLUSION Desert: a radar study. Ibis., 142 : 623 – 634. Our results confirmed that Blondel J (1975). L'analyse des Bousaâda oasis represents an important peuplements d'oiseaux, éléments habitat exploited as wintering grounds, d'un diagnostic écologique : la stopover site during trans-Saharan méthode des échantillonnages migration, and breeding sites for several fréquentiels progressifs. Revue species. Regarding the strategic d'Ecologie (La Terre et la Vie)., geographic situation of this region as a key 29 : 533–589. in the regional scale biodiversity and bird’s Botes A, Zaid A (2002). The economic dynamic this needs further investigations importance of date production and on habitat preferences of birds. international trade In Zaid A, (ed.). Date palm cultivation. FAO REFERENCES Plant Production and Protection Bairlein F. (1992). Recent prospects on Paper no. 156. Rome: Food and trans-Saharan migration of Agriculture Organisation of the songbirds. Ibis., 134: 41–46. United Nations, Pp: 45–56.

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